Activation of c-Abl Kinase Potentiates the Anti-myeloma Drug Lenalidomide by Promoting DDA1 Protein Recruitment to the CRL4 Ubiquitin Ligase

J Biol Chem. 2017 Mar 3;292(9):3683-3691. doi: 10.1074/jbc.M116.761551. Epub 2017 Jan 13.

Abstract

Cullin-RING ligase 4 (CRL4), a complex of Cul4 and DDB1, regulates the cell cycle, DNA damage repair, and chromatin replication by targeting a variety of substrates for ubiquitination. CRL4 is also hijacked by viral proteins or thalidomide-derived compounds to degrade host restriction factors. Here we report that the c-Abl non-receptor kinase phosphorylates DDB1 at residue Tyr-316 to recruit a small regulatory protein, DDA1, leading to increased substrate ubiquitination. Pharmacological inhibition or genetic ablation of the Abl-DDB1-DDA1 axis decreases the ubiquitination of CRL4 substrates, including IKZF1 and IKZF3, in lenalidomide-treated multiple myeloma cells. Importantly, panobinostat, a recently approved anti-myeloma drug, and dexamethasone enhance lenalidomide-induced substrate degradation and cytotoxicity by activating c-Abl, therefore providing a mechanism underlying their combination with lenalidomide to treat multiple myeloma.

Keywords: CRL4; DDA1; c-Abl; cancer biology; cancer therapy; lenalidomide; molecular cell biology; ubiquitin ligase; ubiquitylation (ubiquitination).

MeSH terms

  • Angiogenesis Inhibitors / pharmacology
  • Cell Line, Tumor
  • Cell Survival
  • DNA-Binding Proteins / metabolism*
  • Dexamethasone / pharmacology
  • Gene Expression Regulation, Neoplastic
  • Humans
  • Hydroxamic Acids / pharmacology
  • Indoles / pharmacology
  • Lenalidomide
  • Multiple Myeloma / drug therapy
  • Multiple Myeloma / metabolism
  • Panobinostat
  • Protein Binding
  • Proteolysis
  • Proto-Oncogene Proteins c-abl / metabolism*
  • Thalidomide / analogs & derivatives*
  • Thalidomide / pharmacology
  • Tyrosine / chemistry
  • Ubiquitin-Protein Ligases / metabolism*
  • Ubiquitination

Substances

  • Angiogenesis Inhibitors
  • DDA1 protein, human
  • DDB1 protein, human
  • DNA-Binding Proteins
  • Hydroxamic Acids
  • IL17RB protein, human
  • Indoles
  • Tyrosine
  • Thalidomide
  • Dexamethasone
  • Panobinostat
  • Ubiquitin-Protein Ligases
  • Proto-Oncogene Proteins c-abl
  • Lenalidomide